Associations between the presence of virulence determinants and the epidemiology and ecology of zoonotic Escherichia coli

Abstract

The severity of human infection with pathogenic Escherichia coli depends on two major virulence determinants (eae and stx) that, respectively, produce intimin and Shiga toxin. In cattle, both may enhance colonization, but whether this increases fitness by enhancing cattle-to-cattle transmission in the field is unknown. In E. coli O157, the almost uniform presence of the virulence determinants in cattle isolates prevents comparative analysis. The availability to this study of extensive non-O157 E. coli data, with much greater diversity in carriage of virulence determinants, provides the opportunity to gain insight into their potential impact on transmission. Dynamic models were used to simulate expected prevalence distributions for serogroups O26 and O103. Transmission parameters were estimated by fitting model outputs to prevalence data from Scottish cattle using a Bayesian Markov chain Monte Carlo (MCMC) approach. Despite similar prevalence distributions for O26 and O103, their transmission dynamics were distinct. Serogroup O26 strains appear well adapted to the cattle host. The dynamics are characterized by a basic reproduction ratio (R(0)) of >1 (allowing sustained cattle-to-cattle transmission), a relatively low transmission rate from environmental reservoirs, and substantial association with eae on transmission. The presence of stx(2) was associated with reduced transmission. In contrast, serogroup O103 appears better adapted to the noncattle environment, characterized by an R(0) value of <1 for plausible test sensitivities, a significantly higher transmission rate from noncattle sources than serogroup O26, and an absence of fitness benefits associated with the carriage of eae. Thus, the association of eae with enhanced transmission depends on the E. coli serogroup. Our results suggest that the capacity of E. coli strains to derive fitness benefits from virulence determinants influences the prevalence in the cattle population and the ecology and epidemiology of the host organism.

FIG. 1.

Observed prevalence distributions for E. coli serogroups O26 (black) and O103 (gray) derived from a sample of 6,086 fecal pats from 414 cattle groups. (a) Full dataset; (b) dataset excluding observed zero prevalences, to expose the tails of the distributions.

FIG. 2.

Transmission dynamics of E. coli serogroups O26 (black) and O103 (gray). For a test sensitivity of 0.5, the posterior distributions for the basic reproduction ratio, R₀ (a), and the immigration rate, λ_r (b). For a range of assumed test sensitivities, estimates of the basic reproduction ratio, R₀ (c), and the immigration rate, λ_r (d). The error bars indicate 95% credible intervals.

FIG. 3.

Impact of virulence determinants on transmission. (a) R₀ for E. coli serogroup O26 eae-positive (solid) and eae-negative (dashed) strains. (b) R₀ for E. coli serogroup O103 eae-positive (solid) and eae-negative (dashed-dotted) strains. (c) R₀ for E. coli serogroup O26 stx-positive (solid black), stx-negative (dashed black), stx-positive-and-eae-positive (solid gray), and O26 stx-negative-and-eae-positive (dashed gray) strains. (d) R₀ for E. coli serogroup O26 stx₁-only-positive (gray) and O26 stx₁-and-stx₂-positive (black) strains. The error bars indicate 95% credible intervals and have been slightly displaced for clarity in panels c and d.